diff --git a/crates/handlers/src/views/register/mod.rs b/crates/handlers/src/views/register/mod.rs
index 70d2b2b68..3e9528985 100644
--- a/crates/handlers/src/views/register/mod.rs
+++ b/crates/handlers/src/views/register/mod.rs
@@ -177,13 +177,17 @@ pub(crate) async fn post(
 ) -> Result<Response, InternalError> {
     let user_agent = user_agent.map(|ua| ua.as_str().to_owned());
 
-    let Ok(form) = cookie_jar.verify_form(&clock, form) else {
+    let Ok(mut form) = cookie_jar.verify_form(&clock, form) else {
         // An invalid token most likely comes from a page left open past the CSRF token lifetime
         tracing::debug!("Invalid CSRF token on the registration form, redirecting to a fresh one");
         let destination = Register::from(query.post_auth_action);
         return Ok((cookie_jar, url_builder.redirect(&destination)).into_response());
     };
 
+    // Matrix localparts are lowercase, so a stray capital or surrounding space
+    // isn't worth an error
+    form.username = form.username.trim().to_lowercase();
+
     // Carry the username along so we can prefill it if the user gets to pick
     // one when they come back
     if let Some(provider_id) = &form.provider {
@@ -201,9 +205,8 @@ pub(crate) async fn post(
         };
 
         // The username is carried in a cookie, so its size has to be bounded
-        let username = form.username.trim();
-        let username = if username.len() <= MAX_USERNAME_LENGTH {
-            username
+        let username = if form.username.len() <= MAX_USERNAME_LENGTH {
+            form.username.as_str()
         } else {
             ""
         };
diff --git a/crates/handlers/src/views/register/password.rs b/crates/handlers/src/views/register/password.rs
index 4704806c7..20a7090a5 100644
--- a/crates/handlers/src/views/register/password.rs
+++ b/crates/handlers/src/views/register/password.rs
@@ -364,6 +364,55 @@ mod tests {
         },
     };
 
+    /// The username is trimmed and lowercased before anything checks it
+    #[sqlx::test(migrator = "mas_storage_pg::MIGRATOR")]
+    async fn test_register_normalizes_username(pool: PgPool) {
+        setup();
+        let state = TestState::from_pool(pool).await.unwrap();
+        let cookies = CookieHelper::new();
+
+        let request = Request::get(&*mas_router::Register::default().path_and_query()).empty();
+        let request = cookies.with_cookies(request);
+        let response = state.request(request).await;
+        cookies.save_cookies(&response);
+        response.assert_status(StatusCode::OK);
+        let csrf_token = response
+            .body()
+            .split("name=\"csrf\" value=\"")
+            .nth(1)
+            .unwrap()
+            .split('\"')
+            .next()
+            .unwrap();
+
+        let request = Request::post(&*mas_router::Register::default().path_and_query()).form(
+            serde_json::json!({
+                "csrf": csrf_token,
+                "username": " John ",
+                "email": "john@example.com",
+                "password": "correcthorsebatterystaple",
+                "password_confirm": "correcthorsebatterystaple",
+                "accept_terms": "on",
+            }),
+        );
+        let request = cookies.with_cookies(request);
+        let response = state.request(request).await;
+        response.assert_status(StatusCode::SEE_OTHER);
+        let location = response.headers().get(LOCATION).unwrap();
+        let id = location
+            .to_str()
+            .unwrap()
+            .rsplit('/')
+            .nth(1)
+            .unwrap()
+            .parse()
+            .unwrap();
+
+        let mut repo = state.repository().await.unwrap();
+        let registration = repo.user_registration().lookup(id).await.unwrap().unwrap();
+        assert_eq!(registration.username, "john");
+    }
+
     /// Test the registration happy path
     #[sqlx::test(migrator = "mas_storage_pg::MIGRATOR")]
     async fn test_register(pool: PgPool) {